The Black Yeasts: an Update on Species Identification and Diagnosis Pullulan Produced by Aureobasidium Melanogenum P16
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Current Fungal Infection Reports https://doi.org/10.1007/s12281-018-0314-0 ADVANCES IN DIAGNOSIS OF INVASIVE FUNGAL INFECTIONS (S CHEN, SECTION EDITOR) 11. Liu, N.-N., Chi, Z., Liu, G.-L., Chen, T.-J., Jiang, H., Hu, J., and Chi, Z.-M. (2018). α-Amylase, glucoamylase and isopullulanase determine molecular weight of The Black Yeasts: an Update on Species Identification and Diagnosis pullulan produced by Aureobasidium melanogenum P16. International Journal of 1 1 Biological Macromolecules 117: 727-734. Connie F. Cañete-Gibas & Nathan P. Wiederhold 12. Tang, R.-R., Chi, Z., Jiang, H., Liu, G.-L., Xue, S.-J., Hu, Z., and Chi, Z.-M. (2018). Overexpression of a pyruvate carboxylase gene enhances extracellular liamocin and # Springer Science+Business Media, LLC, part of Springer Nature 2018 intracellular lipid biosynthesis by Aureobasidium melanogenum M39. Process Abstract Biochemistry 69: 64-74. Purpose of review Black yeast-like fungi are capable of causing a wide range of infections, including invasive disease. The diagnosis of infections caused by these species can be problematic. We review the changes in the nomenclature and taxonomy of 13. Chen, T.-J., Chi, Z., Jiang, H., Liu, G.-L., Hu, Z., and Chi, Z.-M. (2018). Cell wall these fungi, and methods used for detection and species identification that aid in diagnosis. integrity is required for pullulan biosynthesis and glycogen accumulation in Recent findings Molecular assays, including DNA barcode analysis and rolling circle amplification, have improved our ability to Aureobasidium melanogenum P16. BBA - General Subjects 1862: 1516-1526. correctly identify these species. A proteomic approach using matrix-assisted laser desorption/ionization time-of-flight mass spectrometry (MALDI-TOF MS) has also shown promising results. While progress has been made with molecular techniques using direct specimens, data are currently limited. Summary Molecular and proteomic assays have improved the identification of black yeast-like fungi. However, improved molecular and proteomic databases and better assays for the detection and identification in direct specimens are needed to improve the diagnosis of disease caused by black yeast-like fungi. Keywords Black yeasts . Diagnosis . Species identification . Cladophialophora . Exophiala . Fonsecaea Phialophora . Rhinocladiella Introduction infections, which are associated with significant morbidity [7••, 8–12]. Significant differences in pathogenicity and viru- Black yeast-like fungi and their filamentous relatives are ca- lence have also been reported between closely related species, pable of causing a wide range of often difficult to treat infec- and this may be a function of the individual species’ ability to tions. Infections caused by members of the order grow at certain temperatures. Those species that are able to Chaetothyriales, under which these fungi fall, include myce- grow at human body temperature (i.e., 37 °C) or higher are toma, chromoblastomycosis, and phaeohyphomycoses. capable of causing systemic or disseminated disease. These Hematogenously disseminated infections can also occur and species include but are not limited to E. dermatitidis, are primarily caused by Exophiala species that are able to E. jeanselmei, E. oligospora, Cladophialophora bantiana, produce yeast-like cells [1–3, 4•]. Although rare, case reports and Fonsecaea species [4•]. In addition to causing infections of endocarditis due to Exophiala species have been reported in in humans, black yeast-like fungi and their filamentous rela- the literature [5, 6], and a recent epidemiologic study also tives are also capable of causing disease in cold-blooded ani- reported one case caused by Fonsecaea pedrosoi [7••]. mals [13]. Species that grow at temperatures between 35 and Other species are capable of causing central nervous system 37 °C often are associated with superficial and cutaneous in- fections in humans but may cause systemic disease in cold- blooded animals. In contrast, mesophilic species, which only grow at temperatures between 27 and 33 °C, are limited to This article is part of the Topical Collection on Advances in Diagnosis of cold-blooded animals, although infections in invertebrates Invasive Fungal Infections have also been reported [14]. * Connie F. Cañete-Gibas The diagnosis of invasive fungal infections remains chal- [email protected] lenging. In many patients with probable or presumed invasive mycoses, fungal cultures are rarely positive, thus hampering the diagnosis of these infections. However, it is known that 1 Fungus Testing Laboratory, Department of Pathology and Laboratory Medicine, University of Texas Health Science Center at San Antonio, delays in diagnosis and initiation of appropriate therapy are 7703 Floyd Curl Drive, San Antonio, TX 78229, USA associated with worse outcomes in patients with invasive Reproduced from Current Fungal Infection Reports (2018). https://doi.org: 10.1007/s12281-018-0314-0 Connie F. Cañete-Gibas: Participant of the 19th UM, 1991-1992. 220 221 Curr Fungal Infect Rep fungal infections [15–17]. Although these studies have pri- Table 1 List of medically important species in the Family marily involved patients with invasive aspergillosis and can- Herpotrichiellaceae and Cyphellophoraceae [21–24] didiasis, it is presumed that delays in appropriate therapy Genus Species would also lead to worse outcomes in patients with infections caused by other fungi. This review discusses the species of Cladophialophora Cladophialophora arxii Cladophialophora bantiana black yeast-like fungi and their filamentous relatives, changes Cladophialophora boppii in their nomenclature, and methods for diagnosis and species Cladophialophora carrionii identification. (formerly Cladophialophora ajelloi) Cladophialophora devriesii Cladophialophora emmonsii Cladophialophora immunda Species of Black Yeast-like Fungi, Their Cladophialophora modesta Filamentous Relatives and Characteristics Cladophialophora mycetomatis Cladophialophora samoensis Cladophialophora saturnica Black yeast-like fungi and their filamentous relatives are Cladophialophora subtilits dematiaceous, non-lichenized fungi characterized by the pres- Cyphellophora Cyphellophora laciniata ence of a dark yeast-like phase that later becomes a mycelial Cyphellophora pluriseptata Cyphellophora suttonii stage [18]. These fungi exhibit slow to moderate growth and Exophiala Exophiala asiatica as previously noted are classified under the ascomycete order Exophiala attenuata Chaetothyriales (subphylum Pezizomycotina). Five families Exophiala bergeri Exophiala castellanii are recognized within this order: Chaetothyriaceae, Exophiala dermatitidis Cyphellophoraceae, Epibryaceae, Herpotrichiellaceae, and (formerly Wangiella dermatitidis) Trichomeriaceae [19••, 20]. Most clinically important species Exophiala equina Exophiala halophila are included in the Family Herpotrichiellaceae and Exophiala jeanselmei Cyphellophoraceae, mainly in the genera Cladophialophora, Exophiala lecanii-corni Cyphellophora, Exophiala, Fonsecaea, Phialophora, and Exophiala mesophila Exophiala oligosperma Rhinocladiella (Table 1)[19••]. Exophiala spinifera Cladophialophora species produce one-celled ellipsoidal Exophiala “siphonis” to fusiform dry conidia arising through blastic, acropetal Exophiala xenobiotica Fonsecaea Fonsecaea pedrosoi (formerly Fonsecaea conidiogenesis and arranged in branched chains [25]. The compacta, a dysgonic mutant or genus Cyphellophora is characterized by having melanized variety of Fonsecaea pedrosoi) thalli with phialidic condiogenesis, phialidic openings inserted Fonsecaea multimorphosa Fonsecaea nubica directly on hyphae or occasionally on flask-shaped Fonsecaea pedrosoi conidiogenous cells, and producing small clusters of oliva- Phialophora Phialophora Americana ceous, septate or non-septate, mostly curved conidia [26]. Phialophora europaea The genus Exophiala is comprised of species that exhibit Phialophora verrucosa Rhinocladiella Rhinocladiella aquaspera smooth or velvety, initially mucoid, black, olivaceous green (formerly Acrotheca aquaspersa) or dark brown colonies [27]. Nearly all species within this Rhinocladiella basitona genus are characterized and recognizable by their production (formerly Ramichloridium basitonum) Rhinocladiella mackenziei of budding cells, and the yeast-to-hyphae transition mostly (formerly Ramichloridium mackenziei) proceeds via torulose hyphae. These species are highly pleo- Rhinocladiella similis morphic, and morphologic characteristics are often deter- mined by factors such as culture media, incubation tempera- ture, and the age of the culture. The genus Fonsecaea includes smooth- and thin-walled, one or occasionally two-celled, el- species that are defined by the presence of indistinct mela- lipsoidal to clavate in shape [21, 30]. nized conidiophores with blunt, dispersed denticles that bear single or short chains of conidia that eventually become un- branched [28]. The genus Phialophora is characterized by Changes in Nomenclature melanized hyphae and by the production of slimy, one- celled conidia in heads from phialides with distinct collarettes Until 2013, polymorphic higher fungi (Dikarya) were allowed [29]. Another genus of black yeast-like fungi Rhinocladiella is to carry multiple names to describe their teleomorphic and comprised of species with sympodial conidiogenesis. The co- anamorphic stages. These stages occur independently, and nidiophores are dark brown, straight, upright, unbranched, their relationship was not always established. The